View metadata, citation and similar papers at core.ac.uk brought to you by CORE + MODEL ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 1/8 provided by University of Debrecen Electronic Archive
1 53 2 54 3 55 e 4 European Journal of Soil Biology xx (2007) 1 8 56 http://www.elsevier.com/locate/ejsobi 5 57 6 Original article 58 7 59 8 Changes of isopod assemblages along an urbane 60 9 e 61 10 suburban rural gradient in Hungary 62 11 63 12 Elisabeth Hornung a,*,Be´la To´thme´re´sz b, Tibor Magura c, Ferenc Vilisics a 64 13 65 a 14 Department of Ecology, SzIU, FVS, Institute for Zoology, H-1400 Budapest, PO Box 2, Hungary 66 b Ecological Institute, University of Debrecen, Hungary 15 c Hortoba´gy National Park Directorate, Debrecen, Hungary 67 16 68 17 Received 13 December 2005; acceptedPROOF 17 January 2007 69 18 70 19 71 20 72 21 Abstract 73 22 74 23 Responses of isopod assemblages to urbanisation were studied along an urbanesuburbanerural gradient representing a decrease 75 24 in the intensity of human disturbance. Pitfall trapping collected six species (Armadillidium vulgare, Porcellio scaber, Porcellium 76 25 collicola, Trachelipus ratzeburgii, Cylisticus convexus, and Trachelipus rathkii). A. vulgare occurred abundantly in all sites reflect- 77 ing the broad tolerance and invasive nature of this species. Indicator species analysis demonstrated that P. scaber and T. rathkii were 26 78 significant quantitative character species for the urban site, while T. ratzeburgii was characteristic for the natural habitats (suburban 27 and rural sites). CANOCO revealed that ground and air temperature show positive correlation with the distribution of P. scaber and 79 28 T. rathkii, and negative correlation with T. ratzeburgii. Nested ANOVA on trap level showed that there were no significant differ- 80 29 ences between the number of isopod species and individuals, and the diversity of isopod assemblages in the three studied areas. 81 30 Significant differences were observed at site level. The results did not support the hypothesis that diversity should decrease in re- 82 31 sponse to habitat disturbance. They also contradicted the intermediate disturbance hypothesis; species richness was not the highest 83 32 in the moderately disturbed suburban area. Multivariate methods detected that the isopod assemblages of the rural and suburban 84 33 areas were relatively similar, while that of the urban area was relatively separated. 85 34 Ó 2007 Elsevier Masson SAS. All rights reserved. 86 35 87 36 Keywords: Oniscidea; Globenet; Increased disturbance hypothesis; Intermediate disturbance hypothesis; Species richness; Diversity; Urbanisation 88 37 89 38 90 39 1. Introduction to suburban and rural forests, including higher air pollu- 91 40 tion and disturbance intensity, the heat island phenom- 92 41 The effects of urbanisation can be explored through enon and the presence or greater abundance of exotic 93 42 investigations of biotic and abiotic changes along species [34,41]. The floristic richness of many urban 94 43 urban-to-rural gradients [27,29]. Such gradients, from habitats frequently exceeds that of less urbanised areas 95 44 densely built inner citiesUNCORRECTED to increasingly rural surround- [45], reflecting the diverse, and mosaic nature of urban 96 45 ings, reflect diminishing intensities of human influence. habitats and the presence of introduced plants. The 97 46 Urban forests are exposed to unique features compared cityeforest ecotone also plays an important role in 98 47 maintaining this diversity [5]. 99 48 100 * Corresponding author. Tel.: þ36 1 478 42 33; fax: þ36 1 478 42 32. Recently, a multi-national research framework has 49 E-mail address: [email protected] (E. Hornung). been initiated to assess and compare the influence of 101 50 102 51 1164-5563/$ - see front matter Ó 2007 Elsevier Masson SAS. All rights reserved. 103 52 doi:10.1016/j.ejsobi.2007.01.001 104
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001 ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 2/8
2 E. Hornung et al. / European Journal of Soil Biology xx (2007) 1e8
105 urbanisation using invertebrates and standardised field (47 350 N21 370 E). The criteria for distinguishing 157 106 methods (Globenet) [30]. Carabids were selected as urban, suburban and rural area were the ratio of the 158 107 the focal taxon, but other taxa (ants, and spiders) have built-up area to the natural habitats. Disturbance was 159 108 also been studied recently within the Globenet frame- estimated based on a 1 1 km unit around the centre 160 109 work [1]. According to the Globenet protocol, we in- of the investigated area. In the urban area the built-up 161 110 volved in our research three kinds of forested habitats area exceeded 60%, in the suburban area it was approx- 162 111 (urban park, suburban forested area, and rural forest), imately 30%, while in the rural area the built-up area 163 112 representing different levels of human disturbance was 0%. The area of the built-up environment and the 164 113 [31]. The target taxon was the terrestrial, surface active natural habitats was measured by the ArcView GIS 165 114 woodlouse assemblage. Isopods are regarded as a useful program using an aerial photograph. 166 115 and reliable monitoring group. They are widespread, 167 116 easily identified and in most cases dominant compo- 2.2. Sampling design 168 117 nents of the macrodecomposer guild in temperate 169 118 regions [32]. Isopods belong to the saprophagous Four sites, at least 50 m apart, were selected within 170 119 components of the soil macrofauna. These organisms each sampling area (urban, suburban, and rural). Iso- 171 120 process the majority of dead organic material and so pods were collected at each site using pitfall traps, ran- 172 121 influence the rate of nutrient release, an important eco- domlyPROOF placing 10 traps at least 10 m apart from each 173 122 system function. The urban fauna can be very diverse, other at each site. This resulted in a total of 120 traps 174 123 often due to introduced, exotic species [18,20]. In this scattered along the urbanerural gradient (3 area 4 175 124 paper, we tested the following predictions for isopods sites 10 traps). The pitfall traps were unbaited, con- 176 125 in urban environments: (1) diversity should be highest sisting of plastic cups (diameter 65 mm, volume 177 126 in the suburban area (IDH e intermediate disturbance 250 ml) containing 75% ethylene glycol as a killing- 178 127 hypothesis); and (2) diversity should decrease from preserving solution. The traps were covered with bark 179 128 a high value in the rural area to a low one in the urban pieces to protect them from litter and rain. Trapped iso- 180 129 area (increasing disturbance hypothesis). We also inves- pods were collected from the end of March to the end of 181 130 tigated the changes in the isopod assemblages along the November 2001. For the purpose of analysis, we pooled 182 131 urbanisation gradient, identified the characteristic and/ samples from the whole year. 183 132 or key species across this gradient, and correlated cer- Ground temperature at 2 cm depth, and air tempera- 184 133 tain environmental variables with the observed pattern ture and relative humidity at the soil surface were mea- 185 134 of isopod abundance and species richness. sured adjacent to each trap monthly on the morning of 186 135 a typical sunny day. The statistical analyses were based 187 136 2. Material and methods on averages. We also estimated the percentage cover of 188 137 leaf litter, decaying wood material, herbs, shrubs and 189 138 2.1. Study area the canopy within a radius of 1 m around each trap 190 139 (see Table 1). 191 140 The study areas were situated in and around the city 192 141 of Debrecen (Eastern Hungary), the second largest city 193 142 of the country. Three forested sampling areas e each 194 143 covering an area of at least 6 ha e were selected along 195 Table 1 144 an urbanisation gradient [16]; this represented urban, Average values ( SE) of the studied environmental factors in the 196 145 suburban and rural areas, according to the Globenet pro- study areas 197 146 tocol [30]. All sampling sites were in forest stands dom- Urban Suburban Rural 198 147 inated by English oak (Quercus robur); distance among 199 Ground temperature 24.9 0.249a 22.3 0.100b 21.6 0.249c 148 the studied areas wasUNCORRECTED at least 1 km [24]. In the urban Air temperature 31.2 0.146a 27.3 0.076b 27.8 0.220c 200 149 park area, there were several asphalt-covered paths Relative humidity 60.4 0.744a 76.6 0.495b 58.9 0.503c 201 150 and the shrub layer was strongly thinned, while in the Cover of leaf litter 21.1 4.152a 57.1 4.181b 21.1 3.207a 202 a a b 151 suburban area the fallen trees were removed, while in Cover of decaying 3.8 0.495 4.2 0.557 11.0 1.442 203 wood material 152 the rural area forest management was only occasional a b c 204 e Cover of herbs 46.5 5.243 29.1 4.108 68.6 3.348 153 at a low-intensity level. The urban rural gradient Cover of shrubs 25.7 3.570a 55.1 3.602b 11.6 2.183c 205 154 extended over a distance of approximately 6 km, from Canopy cover 55.7 3.577a 49.2 3.035a 52.5 3.331a 206 0 0 155 the city centre (47 32 N21 38 E), through the sub- Different letters indicate significant (p < 0.05) differences by ANOVA 207 156 urbs to the neighbouring NagyerdT Forest Reserve using the Tukey’s post hoc test. 208
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001 ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 3/8
E. Hornung et al. / European Journal of Soil Biology xx (2007) 1e8 3
209 2.3. Data analyses Trachelipus rathkii (Brandt, 1833), Trachelipus ratze- 261 210 burgii (Brandt, 1833), Cylisticus convexus (De Geer, 262 211 To test differences in the overall isopod abundance, 1778)], five species and 2720 individuals in the suburban 263 212 species richness, and diversity (Shannon, Simpson, area (A. vulgare, P. collicola, T. rathkii, T. ratzeburgii, 264 213 BergereParker; see [40]) among the three sampling C. convexus), and four species and 2847 individuals 265 214 areas (urban, suburban and rural), and among the 12 in the rural area (A. vulgare, P. collicola, T. rathkii, 266 215 sites, nested analyses of variance (ANOVA) were per- T. ratzeburgii). Analysing the trap-level data (number 267 216 formed using data from the individual traps (sites nested of individuals) by ANOVA we found no significant 268 217 within the sampling areas). The distribution of data used difference in overall isopod abundance (Table 2; 269 218 in the ANOVA models was normal (tested by the Fig. 1A) at the gradient level, but there were significant 270 219 KolmogoroveSmirnov test [39]). differences at site level. 271 220 The composition of the isopod assemblages along 272 221 the urbanerural gradient was compared at trap level 3.1.2. Number of species and diversity indices 273 222 by multidimensional scaling (MDS) based on the num- The general pattern of changes in species richness 274 223 ber of individuals using the BrayeCurtis index of dis- along the gradient is similar to the changes in abun- 275 224 similarity [19]. dance (Table 2; Fig. 1B). We found no significant differ- 276 225 Characteristic species of the urban, suburban and encePROOF in overall isopod species richness. There was no 277 226 rural areas were identified using the IndVal (indicator significant difference in the Shannon-, Simpson- and 278 227 value) procedure [3]. This method identifies quantita- BergereParker diversity along the gradient (Table 2; 279 228 tively the characteristic species of the studied habitat Fig. 2). Significant differences were observed at site 280 229 types, and generates a significance value (p-value) for level for both the Shannon and Simpson diversity 281 230 the strength of association using a randomised compu- indices. 282 231 terised resampling technique. The characteristic value 283 232 (IndVal) of a species is expressed as a product of the 3.2. Isopod assemblage composition along 284 233 specificity and fidelity measures. It receives its maxi- the urbanerural gradient 285 234 mum (100) when all individuals of a species are found 286 235 in a single habitat type (high specificity) and when the There was no marked separation among the sites 287 236 species occurs at all sites of that type (high fidelity) along the urbanerural gradient. The MDS ordination 288 237 [3]. The characteristic species is defined as the most based on the abundance data revealed that the urban 289 238 characteristic species of each habitat type, found mostly assemblage was separated from the suburban and rural 290 239 in that habitat and present in the majority of sites be- 291 240 longing to that habitat. This proved to be a useful 292 241 method to identify the characteristic invertebrate spe- Table 2 293 Nested ANOVA showing differences in isopod diversity, abundance 242 cies in several habitats [4,22,23]. and species richness along the urbanesuburbanerural gradient and 294 243 The relationships between the environmental factors among the 12 sites 295 244 and the abundance and species richness of isopods were Source of df MS Fp 296 245 examined using the CANOCO package [43,44]. The variation 297 246 CANOCO algorithms perform ordinations of traps Shannon diversity Gradient 2 0.0678 1.3230 ns 298 247 and species data, and arrange the ordination according Sites 9 0.0512 3.5755 <0.01 299 248 to the environmental variables that accompany the Error 108 0.0143 300 249 trap data [19]. Simpson diversity Gradient 2 1.3796 1.5376 ns 301 250 Sites 9 0.8972 2.2529 <0.05 302 251 3. Results Error 108 0.3983 303 252 UNCORRECTEDBergereParker Gradient 2 0.6152 1.7406 ns 304 253 3.1. Isopod diversity along the urbanerural gradient diversity Sites 9 0.3534 1.6312 ns 305 254 Error 108 0.2167 306 255 3.1.1. Abundance All species, Gradient 2 0.0089 0.6306 ns 307 256 The total isopod sample consisted of 9115 individuals number of species Sites 9 0.0141 0.6205 ns 308 257 representing six species; 3548 individuals belonging Error 108 0.0228 309 258 to six species were captured in the urban area [Arma- All species, Gradient 2 0.2479 0.4858 ns 310 259 dillidium vulgare (Latreille, 1804), Porcellio scaber number of Sites 9 0.5102 2.2880 <0.05 311 260 Latreille, 1804, Porcellium collicola (Verhoeff, 1907), individuals Error 108 0.2230 312
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001 ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 4/8
4 E. Hornung et al. / European Journal of Soil Biology xx (2007) 1e8
313 A a 365 a a 314 100 0.3 366 315 a 367 a 316 80 a 0.2 368 317 369 318 370 60 0.1 319 371 320 Shannon diversity 372 40 0.0 321 Urban Suburban Rural 373 322 374 Number of individuals a 323 20 2.0 a 375 324 376 a 325 1.5 377 0 326 Urban Suburban Rural 378 327 1.0 379 B 328 a 380 329 a 0.5 381 a Simpson diversity PROOF 330 3.0 382 0.0 331 Urban Suburban Rural 383 332 384 a 333 1.5 a 385 334 a 386 335 1.5 387 336 1.0 388
337 Number of species 389 338 0.5 390 339 391
340 Berger-Parker diversity 392 0.0 0.0 341 Urban Suburban Rural Urban Suburban Rural 393 342 Fig. 1. Mean values ( SE) of overall isopod abundance (A) and Fig. 2. Mean values ( SE) of overall isopod diversity per trap along 394 343 overall isopod species richness (B) per trap along the urbane the urbanesuburbanerural gradient. Different letters indicate signif- 395 344 suburbanerural gradient. Different letters indicate significant icant (p < 0.05) differences based on the LSD (least significant dif- 396 345 (p < 0.05) differences based on the LSD (least significant difference) ference) multiple comparison. 397 multiple comparison. 346 398 347 P. scaber and T. rathkii, and correlated negatively with 399 348 assemblage and the assemblage of the suburban and T. ratzeburgii (Fig. 4). 400 349 urban areas was similar to each other (Fig. 3). 401 350 We identified the quantitative character species of the 4. Discussion 402 351 studied habitat types by the IndVal procedure (Table 3): 403 352 (1) habitat generalists, numerous in all areas (A. vulgare, 4.1. Diversity 404 353 P. collicola); (2) synantropic species (preferring the 405 354 urban area) or species with broad tolerance, either Urbanisation causes several forms of disturbance, 406 355 recorded exclusively (P. scaber) or most abundant in such as alteration, fragmentation and isolation of indig- 407 356 the urban area (T. rathkiiUNCORRECTED); (3) species characteristic of enous habitats, changes in temperature, moisture and 408 357 the suburban area (C. convexus); and (4) species charac- edaphic conditions, and pollution [29]. Gray [6] hypoth- 409 358 teristic for the suburban and rural areas (T. ratzeburgii). esised that in habitats influenced by disturbance, overall 410 359 diversity should decrease. Our results did not support 411 360 3.3. Environmental factors and isopods this hypothesis. The overall species richness and diver- 412 361 sity of isopods were almost as high in the urban area as 413 362 A Canonical Correspondence Analysis (CANOCO) in the rural one. Overall diversity changes along the dis- 414 363 revealed that ground and air temperatures showed pos- turbance gradient (urbanerural gradient) can be com- 415 364 itive correlations with the abundance distributions of plex, because in a group of taxa, species richness may 416
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001 ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 5/8
E. Hornung et al. / European Journal of Soil Biology xx (2007) 1e8 5
417 urban 469 418 suburban 470 419 0.2 rural 471 420 472 421 473 422 0.0 474 423 475 424 -0.2 476 425 477 426 2nd MDS axis 478 427 -0.4 479 428 480 429 481 -0.6 430 -0.6 -0.4 -0.2 0.0 0.2 0.4 482 431 1st MDS axis 483 432 484 433 Fig. 3. Ordination of the isopod assemblages along the studied 485 urbanerural gradient using the BrayeCurtis index of dissimilarity PROOF 434 and MDS ordination. 486 435 487 436 increase or decrease with disturbance depending on Fig. 4. Canonical Correspondence Analysis of the abundance data of 488 437 their habitat preference. Our findings also contradict isopods and the measured environmental variables. Cylisticus con- 489 438 the IDH [2]. Species richness and/or diversity were vexus was omitted because it was represented by only three 490 individuals. 439 not highest in the moderately disturbed suburban area 491 440 as the IDH predicts. This may be because basal species 492 441 in food webs probably conform to this hypothesis, but 5e6 [21]. It is argued that differences in the landscapes 493 442 isopods, considered as decomposers do not [49]. (here: urban, suburban, and rural area) might affect spe- 494 443 Moreover, urban areas do support important pools of cies abundance[13]. However, differences in overall 495 444 biodiversity. Within many urban areas studied in the Oniscidea abundance between sites were not observed. 496 445 United States and Europe, there are places with levels 497 446 of biodiversity that are comparable to the surrounding 4.2. Isopod assemblage composition along 498 447 native habitats (e.g. [28,8,37]). The average isopod spe- the urbanerural gradient 499 448 cies richness in Hungarian deciduous forests is around 500 449 Few studies have been published on the ecological 501 450 Table 3 characteristics of urban isopod assemblages (commu- 502 451 Two-way indicator table showing the species indicator power for the nity structure, diversity and abundance relations) 503 452 habitat clustering hierarchy [18,20]. Similar urbanerural forest surveys, focusing 504 453 IndVal Urban Suburban Rural on the soil macro fauna (earthworms, isopods, and mil- 505 454 All habitat lipedes) are in progress in the framework of the Balti- 506 455 Armadillidium vulgare 95.83 ns 2088/37 2280/39 2218/39 more Ecosystem Studies Long Term Ecological 507 456 Porcellium collicola 80.83 ns 272/31 245/35 226/31 Project, in the United States [7,15,33]. In the Baltimore 508 457 Suburban and rural metropolitan area, the abundance of isopods in the rural 509 458 Trachelipus ratzeburgii 83.62* 16/3 183/36 339/35 forest was extremely low. Most of the isopod species 510 459 Urban and specimens were collected in city parks. Two isopod 511 460 Trachelipus rathkii UNCORRECTED75.07* 1143/31 10/3 64/19 species (C. convexus and T. rathkii) dominated these 512 461 Porcellio scaber 35.00* 28/14 0/0 0/0 samples. C. convexus in Hungary occurred always in 513 462 Suburban low numbers in human influenced habitats. It was also 514 463 Cylisticus convexus 3.33 ns 1/1 2/2 0/0 introduced to North America, where it became one of 515 464 The IndVal column indicates the species indicator value for the corre- the most common oniscid species especially in the 516 465 sponding clustering level, which is the maximum indicator value ob- urban forests of the North-eastern United States [14]. 517 served in all the clustering hierarchy. ns, not significant; *p < 0.05. 466 In the columns for each species, the first value indicates the number of A surprisingly large fraction of the regional fauna 518 467 specimens present and the second value corresponds to the number of may be found in cities [18,20]. In a previous study in 519 468 traps where the species is present, in this sample group. Budapest we found altogether 18 isopod species, of 520
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001 ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 6/8
6 E. Hornung et al. / European Journal of Soil Biology xx (2007) 1e8
521 which five (27%) were introduced. Three species repre- by higher average temperature (heat islands). The neg- 573 522 sented rural, forest characteristic ones [Orthometopon ative correlation of T. ratzeburgii to these factors is ex- 574 523 planum (Budde-Lund, 1885), T. ratzeburgii and plained by the fact that this species prefers unmanaged 575 524 Protracheoniscus politus (C. Koch, 1841)]. A. vulgare habitats, which are usually characterised by lower 576 525 and P. collicola are generalist and expansive in Hun- ground and air temperature. 577 526 gary. They were present in planted, moderately dis- Species distribution, spatial and temporal pattern, 578 527 turbed forests. The species distribution among abundance of isopods may depend on disturbance, on 579 528 localities reflected the degree of anthropogenic impact. food quality and shelter site availability. Proportion of 580 529 C. convexus and Porcellionides pruinosus (Brandt, dicotyledonous plants as good quality food may play 581 530 1833) indicated strong human influence [20]. Urban an important regulating factor in isopod abundance 582 531 habitats are often considered to be hotspots of species [35,36]. The quality of leaf litter did not influence mi- 583 532 introductions [26,42]. Exotic species can easily colo- crohabitat selection of A. vulgare although it had signif- 584 533 nize these heavily disturbed areas. Once established icant affects on its growth and survival. Soil texture and 585 534 they can grow in number and begin to expand their the overall fluctuation of yearly climate had an influ- 586 535 range, occasionally becoming invasive by the general- ence on the species’ spatial distribution [11]. The 587 536 ized statistical ‘‘tens rule’’ [48]. abundance of Trachelipus nodulosus C.L. Koch and 588 537 The exclusive appearance of P. scaber in the urban A. vulgarePROOFproved to be correlated with soil parameters 589 538 park is in accordance with this species’ habitat prefer- and vegetation composition, respectively [12]. 590 539 ence. Contrary to the Atlantic and Mediterranean areas 591 540 of Europe, in Hungary this species can be found only in 4.4. Findings of other Globenet projects 592 541 human settlements, and in and around houses (its Hun- 593 542 garian name, ‘‘cellar bug’’ refers to its most frequent There are published papers about the results of the 594 543 occurrence) where heat island effect succeeds, while Globenet project concerning carabid beetles in five 595 544 it is a species of ubiquitous, eurotopic nature in Britain countries, including Finland, Canada, Bulgaria, Japan 596 545 [10]. Habitat preferences of species may depend on the and Hungary. The average number of individuals and 597 546 biogeographical region. For example the originally species were compared in each project along an e 598 547 East- and Middle-European C. convexus inhabits natu- suburbanerural gradient. In Finland both the number 599 548 ral coastal and different human sites in Britain [9]. of individuals and the number of species increased 600 549 T. rathkii, similarly to A. vulgare has a wide range of significantly from the urban area towards the rural 601 550 habitats in whole Europe which are mainly different area [31]. Another study in Finland reported no signif- 602 551 grasslands and synantropic places. P. collicola is dis- icant difference in the number of individuals, while the 603 552 tributed from northern Greece through Hungary to number of species increased significantly from the ur- 604 553 south-east Germany [38]. In Hungary it has a broad tol- ban towards the rural area [47]. In a third study no sig- 605 554 erance living both in humid grasslands and moderately nificant difference was found neither in the number of 606 555 dry forests, from occasionally inundated gallery forests individuals nor in the number of species [1]. In Canada 607 556 to urban parks. the number of individuals was the highest in the subur- 608 557 The relatively stronger separation of the urban area ban area, while the number of species was the highest in 609 558 from the suburban and rural ones in our study was likely the rural area [31]. In Bulgaria there were no significant 610 559 caused by the higher abundances of the generalist differences neither in the number of individuals nor the 611 560 species. Furthermore, T. ratzeburgii was sensitive to number of species [31]. In Japan both the number of in- 612 561 changes in environmental conditions in the urban area, dividuals and the number of species increased from the 613 562 and it was only abundant in the suburban and rural sites. urban area towards the rural area [17]. In Hungary the 614 563 number of individuals was significantly higher in the ru- 615 564 4.3. Environmental factorsUNCORRECTED and isopods ral area than in the suburban and urban areas, but the 616 565 number of species was significantly lower in the subur- 617 566 Although terrestrial isopods are dependent first of all ban area than in the urban and rural areas during 2001. 618 567 on soil moisture and humidity, here we could use the There were no differences in the number of species be- 619 568 values of indirect factors measured: ground temperature tween the urban and rural area [24]. However, there was 620 569 at 2 cm depth and the air temperature on the surface no significant difference in the number of species along 621 570 were higher in the urban area, which appeared to be the urbanisation gradient in Hungary during 2002 [25]. 622 571 favoured by T. rathkii and P. scaber. These species pre- In spite of that the number of species was not different, 623 572 ferred the urban habitats, which is usually characterised the number of forest specialist species increased 624
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001 ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 7/8
E. Hornung et al. / European Journal of Soil Biology xx (2007) 1e8 7
625 significantly from the urban towards the rural area in [8] J. Hadidian, J. Sauer, C. Swarth, P. Handly, S. Droege, 677 626 both years [24,25]. C. Williams, J. Huff, G. Didden, A citywide breeding survey 678 e 627 In Finland spider species were also studied in the for Washington, DC, Urban Ecosys. 1 (1997) 87 102. 679 [9] P.T. Harding, S.L. Sutton, Woodlice in Britain and Ireland: Dis- 628 Globenet project. There were no significant differences tribution and Habitat, Lavenham Press, Great Britain, 1985. 680 629 neither in the number of individuals nor in the species [10] P.T. Harding, S.P. Rushton, M.D. Eyre, S.L. Sutton, Multivari- 681 630 richness [1]. ate analysis of British data on the distribution and ecology of 682 631 The outcome of these studies is rather diverse. It is terrestrial Isopoda, in: P. Juchault, J.P. Mocquard (Eds.), Bio- 683 632 likely, that the number of individuals and the number logy of Terrestrial Isopods, Third International Symposium, 684 Universite de Poitiers, Poitiers, 1990, pp. 65e72. 633 of species are not the most appropriate measures char- [11] F. Heinzelmann, C.S. Crawford, M.C. Molles Jr., 685 634 acterising the effect of urbanisation. Groups of species M.R. Warburg, Microhabitat selection by Armadillidium vul- 686 635 with different ecological characteristics (forest special- gare in a riparian forest: lack of apparent influence by leaf litter 687 636 ists, open habitat species, generalists, etc.) influenced in food quality, in: M.A. Alikhan (Ed.), Terrestrial Isopod Biology, 688 e 637 a strikingly different way by the urbanisation. These A.A. Balkema, Rotterdam, Brookfield, 1995, pp. 133 143. 689 [12] E. Hornung, Isopod distribution in a heterogeneous grassland 638 subtle differences in the ecological behaviour and/or habitat, in: P. Juchault, J.P. Mocquard (Eds.), Third Symposium 690 639 habitat preference of the species should be considered on the Biology of Terrestrial Isopods, Universiteit de Poitiers, 691 640 during the studies. The habitat affinity indices may pro- France, 1991, pp. 73e79. 692 641 vide a useful way to quantify these ecological character- [13] E.PROOF Hornung, Comparison of different grassland types based on 693 642 istics of the assemblages [46]. isopod communities, in: L. Zombori, L. Peregovits (Eds.), Proc. 694 4th ECE/XIII, SIEEC, Go¨do¨llT, 1992, pp. 741e746. 643 [14] E. Hornung, K. Szlavecz, Establishment of a mediterranean 695 644 696 Acknowledgments isopod (Chaetophiloscia sicula Verhoeff, 1908) in a north 645 American temperate forest, Crustaceana Monogr. 2 (2003) 697 646 181e189. 698 We wish to express our thanks to Z. Elek (DE, 647 [15]
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001 ARTICLE IN PRESS EJSOBI2173_proof 7 March 2007 8/8
8 E. Hornung et al. / European Journal of Soil Biology xx (2007) 1e8
729 K. Medley, Ecosystem processes along an urban-to-rural gradi- [39] R.R. Sokal, F.J. Rohlf, Biometry, Freeman, New York, USA, 761 730 ent, Urban Ecosys. 1 (1997) 21e36. 1995. 762 731 [28] M.L. McKinney, Urbanization, biodiversity, and conservation, [40] T.R.E. Southwood, P.A. Henderson, Ecological Methods, 763 732 Bioscience 52 (2002) 883e890. Blackwell Science, 2000. 764 733 [29] J. Niemela¨, Ecology and urban planning, Biodivers. Conserv. 8 [41] J.R. Spence, D.H. Spence, Of ground beetles and men: intro- 765 734 (1999) 119e131. duced species and the synanthropic fauna of western Canada, 766 735 [30] J. Niemela¨, J. Kotze, A. Ashworth, P. Brandmayr, K. Desender, Mem. Entomol. Soc. Can. 144 (1988) 151e168. 767 736 T. New, L. Penev, M. Samways, J. Spence, The search for com- [42] H. Sukopp, Urban ecology and its application in Europe, in: 768 737 mon anthropogenic impacts on biodiversity: a global network, H. Sukopp, S. Hejny (Eds.), Urban Ecology, SPB Academic 769 738 J. Insect Conserv. 4 (2000) 3e9. Publ., The Hague, The Netherlands, 1990. 770 739 [31] J. Niemela¨, J.D. Kotze, S. Venn, L. Penev, I. Stoyanov, J. Spence, [43] C.J.F. ter Braak, Canonical correspondence analysis: a new 771 740 D. Hartley, E. Montes de Oca, Carabid beetle assemblages (Cole- eigenvector method for multivariate direct gradient analysis, 772 741 optera, Carabidae) across urbanerural gradients: an international Ecology 67 (1986) 1167e1179. 773 742 comparison, Landscape Ecol. 17 (2002) 387e401. [44] C.J.F. ter Braak, P. Sˇmilauer, CANOCO Reference Manual and 774 743 [32] M.G. Paoletti, M. Hassall, Woodlice (Isopoda, Oniscidea): their User’s Guide to Canoco for Windows. Software for Canonical 775 744 potential for assessing sustainability and use as bioindicators, Community Ordination (version 4), Centre for Biometry and 776 745 Agr. Ecosyst. Environ. 74 (1999) 157e165. Microcomputer Power, Wageningen and Ithaca, 1998. 777 746 [33] M. Parlange, The city as ecosystem, Bioscience 48 (1998) 581e585. [45] T. Tonteri, Y. Haila, Plants in a boreal city: ecological charac- 778 747 [34] R.V. Pouyat, M.J. McDonnell, S.T.A. Pickett, Litter decomposi- teristics of vegetation in Helsinki and its surroundings, southern 779 748 tion and nitrogen mineralization in oak stands along an urbane Finland, Ann. Bot. Fenn. 27 (1990) 337e352. 780 749 rural land use gradient, Urban Ecosys. 1 (1997) 117e131. [46] B.PROOF To´thme´re´sz, T. Magura, Affinity indices for environmental 781 750 [35] S.P. Rushton, M. Hassall, Food and feeding rates of the terres- assessment using carabids, in: G.L. Lo¨vei, S. Toft (Eds.), 782 751 trial isopod Armadillidium vulgare (Latreille), Oecologia 57 European Carabidology 2003, Proceedings of the 11th 783 752 (1983) 415e419. European Carabidologists’ Meeting, DIAS Report, No. 114, 784 753 [36] S.P. Rushton, M. Hassall, Effects of food quality on isopod dy- Flakkebjerg (2005), pp. 345e352. 785 754 namics, Funct. Ecol. 1 (1987) 359e367. [47] S.J. Venn, D.J. Kotze, J. Niemela¨, Urbanization effects on 786 755 [37] M. Schaefer, K. Kock, Zur O¨ kologie der Arthropodenfauna carabid diversity in boreal forests, Eur. J. Entomol. 100 787 756 einer Stadtlandschaft und ihrer Umgebung am Laufka¨fer (2003) 73e80. 788 757 (Carabidae) und Spinnen (Araneida), Anz. Schadlingskde [48] M. Williamson, A. Fitter, The varying success of invaders, 789 758 Pflanzenschutz Umweltschutz 52 (1979) 85e90. Ecology 77 (1996) 1666e1670. 790 759 [38] H. Schmalfuss, World catalog of terrestrial isopods (Isopoda: [49] J.T. Wootton, Effects of disturbance on species diversity: 791 760 Oniscidea), Stuttg. Beitr. Natkd. Ser. A (Biol.) 654 (2003) 1e341. a multitrophic perspective, Am. Nat. 152 (1998) 803e825. 792
UNCORRECTED
Please cite this article in press as: E. Hornung et al., Changes of isopod assemblages along an urbanesuburbanerural gradient in Hungary, Eur. J. Soil Biol. (2007), doi:10.1016/j.ejsobi.2007.01.001